Microbial succession in a marine sediment: Inferring interspecific microbial interactions with marine cable bacteria

Abstract

Cable bacteria are long, filamentous, multicellular bacteria that grow in marine sediments and couple sulfide oxidation to oxygen reduction over centimetre-scale distances via long-distance electron transport. Cable bacteria can strongly modify biogeochemical cycling and may affect microbial community networks. Here we examine interspecific interactions with marine cable bacteria (Ca. Electrothrix) by monitoring the succession of 16S rRNA amplicons (DNA and RNA) and cell abundance across depth and time, contrasting sediments with and without cable bacteria growth. In the oxic zone, cable bacteria activity was positively associated with abundant predatory bacteria (Bdellovibrionota, Myxococcota, Bradymonadales), indicating putative predation on cathodic cells. At suboxic depths, cable bacteria activity was positively associated with sulfate-reducing and magnetotactic bacteria, consistent with cable bacteria functioning as ecosystem engineers that modify their local biogeochemical environment, benefitting certain microbes. Cable bacteria activity was negatively associated with chemoautotrophic sulfur-oxidizing Gammaproteobacteria (Thiogranum, Sedimenticola) at oxic depths, suggesting competition, and positively correlated with these taxa at suboxic depths, suggesting syntrophy and/or facilitation. These observations are consistent with chemoautotrophic sulfur oxidizers benefitting from an oxidizing potential imparted by cable bacteria at suboxic depths, possibly by using cable bacteria as acceptors for electrons or electron equivalents, but by an as yet enigmatic mechanism.

Biogeochemical impacts of fish farming on coastal sediments: Insights into the functional role of cable bacteria

“…In fact, micro-aerophilic, sulfur-oxidizing taxa [Sulfurimonas and Thioalkalispira-Sulfurivermis, (Sorokin et al, 2002;Takai et al, 2006)] were found to increase 9 and 18 times (respectively), exhibiting higher average relative abundances (7.3 and 4.7%, respectively) in our lab incubation compared to field sediments (Supplementary Figure 3). Likewise, a positive correlation between sulfur-oxidizing Gammaproteobacteria (Thiogranum and Sedimenticola) and cable bacteria was recently observed in sulfidic sediments from seasonally hypoxic area in Chesapeake bay (Liau et al, 2022). The potential for improved recovery of fish farm sediments, via efficient sulfide removal by a diverse microbial community enhanced by cable bacteria, is evident from our study.…”

“…Additionally, Magnetovibrio, a motile, microaerophilic, sulfur oxidizer (Bazylinski et al, 2013), increased 20 times in abundance in the lab incubations compared to field sediments (Supplementary Figure 3). Similar positive correlation between Magnetovibrio and cable bacteria have been reported in lab incubations, suggesting an adaptive advantage for this microbe potentially linked to the microscale geochemical fluctuations created by cable bacteria activity, in particular related to iron availability (Liau et al, 2022).…”

“…Indeed, sediments from LPP sites at 50 m distance, and to a lesser degree from SPP, showed a diversity and relative abundance of cable bacteria similar to that found in the lab incubations ( Figure 5D and Supplementary Table 4 ). In sediments with a clear e-SOx signature, cable bacteria can account for 0.6% up to 7% of the total 16S rRNA gene sequences, and as low as 0.2% in oxic layers or in suboxic sediment when the e-SOx signal is weakening ( Klier et al, 2018 ; Otte et al, 2018 ; Geelhoed et al, 2020 ; Dam et al, 2021 ; Liau et al, 2022 ). A recent study further shows a 10-fold higher percentage of cable bacteria sequences, when comparing DNA-based to RNA-based 16S rRNA genes in the same sediment sample ( Liau et al, 2022 ).…”

“…Thus, the development of e-SOx may still occur within the similar timeframe as in our lab incubations. Furthermore cable bacteria act as ecosystem engineers by influencing the geochemical cycling in sediments via indirect stimulation of microbial processes such as sulfate reduction, hydrocarbon degradation (toluene, alkanes, and PAHs), iron cycling and denitrification (Müller et al, 2016;Otte et al, 2018;Kessler et al, 2019;Marzocchi et al, 2020;Sandfeld et al, 2020;Liu et al, 2021;Huang et al, 2022;Liau et al, 2022). Indeed, some of the genera that positively correlated to e-SOx activity in our lab incubations (Figure 4) may perform sulfate reduction (Desulfocapsa, SEEP-SRB1, and Sva0081), denitrification (Thauera, Dechloromonas, Rhodoferex, Zoogloea, and Acidovorax) and iron oxidation (Acidovorax).…”

“…In this unique bacterial metabolism, sulfide oxidation is supported by long-distance electron transport over centimeters ( Nielsen and Risgaard-Petersen, 2015 ; Meysman, 2018 ). Cable bacteria activity stimulates various other microbial processes, such as sulfate reduction, denitrification, and chemoautotrophy ( Vasquez-Cardenas et al, 2015 ; Kessler et al, 2019 ; Sandfeld et al, 2020 ; Liau et al, 2022 ) promotes cryptic sulfur cycling, and alters the cycling of phosphorous, manganese and heavy metals in sediment ( Rao et al, 2014 ; van de Velde et al, 2016 ). e-SOx can also play a crucial role in the prevention of euxinic bottom waters.…”